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Perirhinal Cortex Lesions Produce Retrograde Amnesia for Spatial Information in Rats: Consolidation Or Retrieval? Juan M.J

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Perirhinal Cortex Lesions Produce Retrograde Amnesia for Spatial Information in Rats: Consolidation Or Retrieval? Juan M.J Downloaded from learnmem.cshlp.org on October 2, 2021 - Published by Cold Spring Harbor Laboratory Press Research Perirhinal cortex lesions produce retrograde amnesia for spatial information in rats: Consolidation or retrieval? Juan M.J. Ramos1 Departamento de Psicología Experimental y Fisiología del Comportamiento, Facultad de Psicología, Campus de Cartuja, Universidad de Granada, Granada 18071, Spain Several lines of evidence in humans and experimental animals suggest that the hippocampus is critical for the formation and retrieval of spatial memory. However, although the hippocampus is reciprocally connected to adjacent cortices within the medial temporal lobe and they, in turn, are connected to the neocortex, little is known regarding the function of these cortices in memory. Here, using a reference spatial memory task in the radial maze, we show that neurotoxic perirhinal cortex lesions produce a profound retrograde amnesia when learning–surgery intervals of 1 or 50 d are used (Experiment 1). With the aim of dissociating between consolidation and retrieval processes, we injected lidocaine either daily after training (Experiment 2) or before a retention test once the learning had been completed (Experiment 3). Results show that reversible perirhinal inactivation impairs retrieval but not consolidation. However, the same procedure followed in Experiment 2 disrupted consolidation when the lidocaine was injected into the dorsal hippocampus. The results of Experiment 4 rule out the possibility that the deficit in retrieval is due to a state-dependent effect. These findings demonstrate the differential contribution of various regions of the medial temporal lobe to memory, suggesting that the perirhinal cortex plays a key role in the retrieval of spatial information for a long period of time. Since the discovery of the dramatic retrograde amnesia induced network of structures (Ross and Eichenbaum 2006; Texeira et al. by bilateral damage to the medial temporal lobe in the patient 2006; Ji and Wilson 2007). However, the anatomical routes by HM, the hippocampus and its related cortices (entorhinal, peri- which the hippocampal region accesses the neocortical represen- rhinal, and postrhinal) have been the subject of a great number tation of episodes or facts are not known. In terms of connectiv- of studies about the brain systems involved in long-term memory ity, the PRC is ideally located to link the hippocampus with as- formation and retrieval (Milner et al. 1998; Squire et al. 2004; sociation cortices involved in different aspects of spatial cogni- Frankland and Bontempi 2005). Over the last 15 years, many tion (Scharfman et al. 2000). Supporting this idea, several studies clinical observations in humans, for whom detailed neuropath- have shown that prefrontal cortex or amygdala inputs can facili- ological and neuropsychological information is available, have tate the transfer of hippocampal activity to the neocortex via an revealed that after limited lesions to the CA1 field of the hippo- enhancement of entorhinal to perirhinal communication, so it campus, retrograde amnesia is temporally graded, covering only may be that the perirhinal cortex is a necessary interface between a few years (Zola-Morgan et al. 1986; Manns et al. 2003). Inter- the hippocampus and a distributed neocortical network for long- estingly, when the damage occurs in the hippocampus plus the term memory (Paz et al. 2006, 2007). In addition, functional adjacent cortices, some studies have found a more profound and studies in which the PRC is hyperactivated by means of excito- extended retrograde amnesia, sometimes lasting decades (Reed toxic or electrolytic lesions have demonstrated increased c-Fos and Squire 1998; Bayley et al. 2006; for review, see Squire and expression in the parietal, retrosplenial, and frontal cortices, re- Bayley 2007), while others have shown an ungraded memory loss gions that are all involved in the long-term representation of (Moscovitch et al. 2006). The differential magnitude and exten- spatial memory (Glenn et al. 2005; see also Maviel et al. 2004). sion of retrograde amnesia following limited hippocampal dam- Several studies have examined, with different behavioral age versus large medial temporal lobe lesions suggest that the paradigms and species, the effect of PRC lesions on memory con- adjacent cortices have an essential function in memory forma- solidation or retrieval. When object discrimination problems and tion or retrieval. Thus, although several lines of research indicate permanent lesions have been used, results have been inconsis- that the hippocampus is necessary for the initial retrieval and tent. Some studies have found a profound graded retrograde am- consolidation of declarative memory (for review, see Frankland nesia (Wiig et al. 1996; Kornecook et al. 1999) and others only a and Bontempi 2005), the specific contribution of the different mild, transient amnesia (Mumby and Glenn 2000). In monkeys, cortices in the medial temporal lobe to the formation of long- rhinal cortex removal produced retrograde amnesia for two sets term memory or retrieval is not yet well understood. of object discrimination problems (each set having 60 problems) The present study focuses on the perirhinal cortex (PRC), learned 16 wk or 1 wk before surgery; however, the lesions did and it uses a spatial paradigm in rats. It has been proposed that not disrupt postoperative acquisition and retention of similar the encoding, retrieval, and consolidation of declarative memory problems, suggesting that this cortex is critical for consolidation rely on interactions between the hippocampus and a cortical and/or retrieval of object discrimination problems (Thornton et al. 1997). Other investigations, using reversible lesions, have demonstrated the involvement of the PRC in encoding, retrieval, 1Corresponding author. and consolidation stages in object-recognition tasks (Winters E-mail [email protected]; fax 34-958-246239. and Bussey 2005a,b). In relation to contextual memory, Burwell Article is online at http://www.learnmem.org/cgi/doi/10.1101/lm.1036308. et al. (2004) showed clearly that the PRC is involved in the stor- 15:587–596 © 2008 Cold Spring Harbor Laboratory Press 587 Learning & Memory ISSN 1072-0502/08; www.learnmem.org Downloaded from learnmem.cshlp.org on October 2, 2021 - Published by Cold Spring Harbor Laboratory Press Retrograde amnesia after perirhinal cortex lesion age and/or retrieval of the memory for contextual fear for at least Histology 100 d after learning. In contrast with the foregoing, however, Tissue damage was microscopically identified by marked thin- there has been no observation of a consistent retrograde amnesia ning of the cortex, necrosis, or missing tissue. No important dif- in tasks using complex contextual information, particularly in ferences were found between the histological results of the four allocentric tasks, where subjects must recall spatial relations be- lesioned groups used in this experiment: perirhinal cortex le- tween landmarks in order to locate a goal. In these studies only a sions/relearning 1 d (PRC-rl 1 d), perirhinal cortex lesions/ slight and transient retrograde amnesia in early probe trials has relearning 50 d (PRC-rl 50 d), perirhinal cortex lesions/learning 1 been observed in the Morris water maze (Mumby and Glenn d (PRC-l 1 d), and perirhinal cortex lesions/learning 50 d (PRC-l 2000; Glenn et al. 2003). 50 d). The lesions, aimed at areas 35 and 36, were generally lim- One problem with the above studies is that lesions made to ited to the target area, creating a longitudinal groove on both the PRC before training cause a profound anterograde amnesia in sides of the rhinal fissure (Fig. 1). In general, the lesion affected object-recognition memory and contextual fear tasks (Bucci et al. the six layers of the PRC and did not reach (except in two animals 2000; Gaffan et al. 2000; Murray et al. 2007). Thus, with these belonging to group PRC-l 50 d) the postrhinal cortex. In four paradigms, when the lesions are made after the training and ret- cases, the cellular damage affected partially the CA1 field bilat- rograde amnesia is observed, it is difficult to determine if the erally in the ventral hippocampus. In 20% of the animals, the lesions have affected the performance of the task or a process of lateral entorhinal cortex was minimally affected to varying de- consolidation and/or retrieval. In relation to spatial memory, al- grees. When the lateral entorhinal cortex was partially lesioned though there is debate regarding the function of the PRC in ac- (from 3% to 17%), the damaged area was intermediate, between quisition (Muir and Bilkey 2001; Aggleton et al. 2004), several 4 and 5.5 mm posterior to bregma according to the Paxinos and studies have shown that rats with PRC lesions have intact acqui- Watson (1998) atlas. Apparently, in no case (except in the two sition in a radial maze (Bussey et al. 1999; see also Winters et al. aforementioned subjects with partial postrhinal lesions) did the 2004 in a Y-maze). For this reason, the present study uses a spatial most caudal portion of the PRC suffer lesions, and the dorsolat- reference memory test in a four-arm plus-shaped maze, for which eral band of the entorhinal cortex was spared in all cases. In the our laboratory has previously shown the absence of deficits in latter region, spatially modulated neurons have been described acquisition/performance following perirhinal lesions (Ramos recently, and lesion studies have shown its involvement in spa- 2002). In sum, using a hippocampal-dependent spatial reference memory paradigm (Ramos 2000, see Experiment 1), the principal aim of the present study was to test the idea that the PRC influ- ences spatial memory formation or retrieval. Results Experiment 1: Neurotoxic lesions of the perirhinal cortex 1 or 50 d after learning The aim of this experiment was to investigate whether damage to the PRC produces retrograde amnesia in rats that had learned a reference spatial memory test presurgically. A four-arm plus- shaped maze was used in such a way that three arms were for starting and the fourth was the goal arm.
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